Negative Impacts and Allelopathic Potential of the Ephemeral Invasive Ranunculus Ficaria

1 Impacts of Lesser Celandine23 Guilty in the Court of Public Opinion: Testing Presumptive Impacts of Lesser Celandine4 (Ranunculus ficaria)56 Kendra A. Cipollini and Kelly D. Schradin*7 *Associate Professor and Undergraduate Student, Wilmington College, Wilmington, OH8 45177. Corresponding author’s E-mail: [email protected].9 Phone: 937-382-6661 ext. 367, Fax: 937-383-85301011Information about invasive species can be based primarily on anecdotal evidence, indicating the 12need for further information. Lesser celandine is an ephemeral riparian plant species that is 13presumed invasive in the United States, despite the lack of any published information on its 14impacts. We examined if lesser celandine negatively affected the growth and reproduction of the 15native jewelweed and, if so, whether it is by allelopathy, nutrient competition or some 16combination thereof. We performed a fully-factorial field experiment in the field, manipulating 17the presence of lesser celandine, nutrients, and allelopathy with the use of activated carbon. The 18presence of lesser celandine tended to negatively affect survival of jewelweed. In the absence of 19carbon, lesser celandine significantly decreased seed production, illustrating the negative impact 20of lesser celandine. In the presence of carbon, there was no effect of lesser celandine, suggesting 21that carbon may have ameliorated the negative allelopathic effect of lesser celandine. Nutrient 22competition did not show strong effects. We found that the negative impacts of this ephemeral 1 23species persist well beyond its early growing season, which calls into question previous 24assumptions about lesser celandine exerting effects primarily on other ephemeral species. 25Nomenclature: Lesser celandine, Ranunculus ficaria L. ssp. bulbifer, jewelweed, Impatiens 26capensis Meerb. 27Key words: Allelopathy, ephemeral, Ficaria verna, fig buttercup, pilewort, vernal.2 28 Invasive species threaten biodiversity on a global scale (Wilcove et al. 1998; McGeoch et29al. 2010) and are defined as those species that cause or have the potential to cause economic or 30environmental harm, weighed against their benefits (NISC 2006). Most naturalized plants are 31introduced through the horticultural industry (Mack and Erneberg 2002) and some can still be 32purchased in some instances despite their invasive status (Harris et al. 2009; Axtell et al. 2010). 33However, only a portion of naturalized species are actually categorized as invasive (Milbau and 34Stout 2008). As a result, there is much interest in characterizing the species traits and 35introduction routes that make a species invasive (Lambdon et al. 2008; Milbau and Stout 2008; 36van Kleunen et al. 2010). Yet, in many of these studies the methods by which species are 37identified as invasive are vague and based on expert opinion and anecdotal evidence, with little 38scientific evidence (Blossey 1999). Further, even when there is some published information, the 39impacts of an invasive species can be overstated by the popular press (Lavoie 2010), which may 40lead to inappropriate response strategies or undue focus. The lack of information on the impact 41of invasive species and on the possible mechanism of impact is an obstacle to effectively 42prioritizing the control of invasive species during a time of dwindling resources. 43 Invasive plant species can negatively impact native species through a variety of 44mechanisms (Levine et al. 2003). Invasive species can simply outcompete native species for 45above- and/or below-ground resources (e.g., Kueffer et al. 2007; Cipollini et al. 2008a; 46Galbraith-Kent and Handel 2008). Enhanced nutrient acquisition can lead to invasive species 47success. For example, Centaurea maculosa acquired more phosphorus than surrounding native 48species which may have increased competitive success (Thorpe et al. 2006). Additionally, 49Leishman and Thomson (2005) found that invasive species had greater responses to nutrient 50addition than native species, thus outcompeting the natives in nutrient-rich environments.3 51 Another mechanism by which invasive species affect native communities is allelopathy 52(Hierro and Callaway 2003; Ens et al. 2009). Most plants produce secondary compounds 53(Ehrenfeld 2006) that can affect an adjacent plant either directly (Cipollini et al. 2008b) or 54indirectly through changing soil ecology (Stinson et al. 2006; Mangla et al. 2008). Some 55allelopathic chemicals that have no negative impact in their native environment may have 56negative effects in an invaded community, a mechanism coined the “novel weapons hypothesis” 57(Callaway and Aschehoug 2000; Callaway and Ridenour 2004; Callaway et al. 2008; Thorpe et 58al. 2009). Discovering impacts due to allelopathy can be done with careful experimentation 59(Inderjit and Callaway 2003). Allelopathic effects have been studied using activated carbon (e.g.,60Ridenhour and Callaway 2001; Cipollini et al. 2008a). Activated carbon adsorbs organic 61compounds, including allelochemicals (Ridenour and Callaway 2001). Addition of carbon can 62also has effects on soil properties and plant growth in potting soil (Lau et al. 2008; Weisshuhn 63and Prati 2009). Addition of nutrients is thought to help ameliorate any fertilizing effects of the 64addition of activated carbon (Inderjit and Callaway 2003). Activated carbon may also serve as a 65restoration tool to change soil conditions in invaded soils (Kulmatiski and Beard 2006; 66Kulmatiski 2010).67 Lesser celandine (Ranunculus ficaria L., Ranunculaceae), is a groundcover native to 68Europe (Taylor and Markham 1978; Sell 1994), which appears to be affecting native plants in 69forested floodplains in many US states (Swearingen 2005). There are five known subspecies, all 70of which are found in the US (Post et al. 2009). Ranunculus ficaria was first recorded naturalized71in the US in 1867 (Axtell et al. 2010). As it is still being marketed by the nursery industry 72(Axtell et al. 2010), it was likely imported for horticultural purposes. It was recognized as a 73naturalized species in the Midwest in the 1980’s (Rabeler and Crowder 1985) and in southern 4 74states more recently (Krings et al. 2005, Nesom 2008). Ranunculus ficaria is currently 75documented in at least 21 US states, the District of Columbia, and 4 Canadian provinces (USDA 762010). It has been identified as invasive in 9 states and the District of Columbia and is banned in 77Massachusetts and Connecticut as a noxious weed (Axtel et al. 2010). 78 Ranunculus ficaria emerges before most native spring species, which may provide it 79with a competitive advantage. Once established, it spreads rapidly across the forest floor to form 80a dense monoculture, which native species seemingly cannot penetrate (Swearingen 2005). 81Hammerschlag et al. (2002) reported that R. ficaria created a monoculture in the Rock Creek 82floodplain in Washington, DC and few native species re-colonized after its removal. It is thought83that R. ficaria, as a spring ephemeral, has impacts primarily on other spring ephemerals 84(Swearingen 2005). However, most all information on R. ficaria as an invasive species is 85primarily anecdotal in nature. Unpublished and preliminary data indicate that presence of R. 86ficaria is associated with reduced abundance and richness of native species (Hohman 2005). 87Unpublished experiments have shown that Ranunculus ficaria exhibits direct allelopathic effects 88on germination of some native species (K. A. Cipollini, personal communication), indicating that89R. ficaria may have negative effects beyond the spring time period through lingering allelopathic90effects. 91 For our study, we examined if R. ficaria negatively affects the growth and reproduction 92of the native annual jewelweed (Impatiens capensis Meerb., Balsaminaceae) and, if so, whether 93it is by allelopathy, nutrient competition or some combination thereof. In the field we performed 94a fully-factorial experiment with the treatments of R. ficaria (present and absent), carbon 95(present and absent), and nutrient addition (present and absent). We expected that the presence of96R. ficaria would have an overall negative impact, that addition of nutrients would have an overall5 97positive impact and that addition of carbon would have no overall effect on the performance of I.98capensis. If allelopathy were important, we expected to see a significant carbon by R. ficaria 99interaction and, if nutrient competition were important, we expected to see a significant nutrient 100by R. ficaria interaction on I. capensis response variables. 101102103104 Materials and Methods105106 We performed the study in 2009 at Hamilton County Park District’s Winton Woods in 107Cincinnati, Ohio, USA in an area invaded by R. ficaria ssp. bulbifer, a subspecies that forms 108asexual bulbils (Post et al. 2009). The study area was found in a floodplain along Westfork Mill 109Creek. We set up the experiment on 24 April, choosing an area with a uniform coverage of R. 110ficaria. We fenced the entire site using deer fencing to prevent trampling and/or herbivory. We 111used a fully factorial design with the main factors of: presence/absence of R. ficaria, 112presence/absence of activated carbon and presence/absence of additional nutrients, replicated 8 113times (2 R. ficaria levels x 2 carbon levels x 2 nutrient levels x 8 replicates = 64 experimental 114units). The treatment combinations were haphazardly assigned to each plot and each plot was 115located approximately 25 cm apart. We tested the effects of these treatment combinations on the 116target plant I. capensis. We chose I. capensis because of the overlap in habitat and distribution 117with R. ficaria. Another advantage is that reproduction can be measured in this annual species. 118Additionally, I. capensis has served as a model organism in previous studies of invasive species 6 119effects (e.g., Cipollini et al. 2008a; Cipollini et al. 2009; Cipollini and Hurley 2009). All I. 120capensis seedlings were obtained in an immediately adjacent area free of R. ficaria. 121 In the R. ficaria-present treatments, we removed R. ficaria and planted them back in place 122while transplanting I. capensis seedlings. In R. ficaria-absent treatments, we removed the R. 123ficaria completely before transplanting I. capensis. In activated carbon-present treatments, we 124worked 10 ml of activated carbon1 into the top 8 cm of soil of each plot. This ratio of activated 125carbon to soil volume has been shown to mitigate allelopathic effects in previous research 126(Cipollini et al. 2008a; Ridenour and Callaway 2001). In nutrient-addition treatments, we worked127the manufacturer-recommended amount of 1.5 teaspoons of Scotts Osmocote2 slow-release 128fertilizer in the top 8 cm of soil in each plot. We disturbed the soil in each subplot regardless of 129treatment combination to control for soil disturbance effects. On May 1 we replaced any I. 130capensis transplants that did not survive, presumably due to transplant shock. We measured the 131height of each seedling when transplanted. The number of fruits, number of seeds and survival 132(days to death) of the seedlings were recorded once each week. Height and stem diameter 133(measured directly beneath bottom node with a digital caliper) was measured. Ranunculus 134ficaria had lost all of its foliage by 2 June (week 6) and the leaf litter had decomposed by 12 135June (week 8), leaving the bulbils exposed on the soil surface. Measurements began on 5 May 136and ended on 28 August (week 18). 137 We performed a series of Analysis of Variances (ANOVAs) on the I. capensis response 138variables, using the full model with fixed factors of nutrients (+/-), R. ficaria (+/-) and carbon 139(+/-). We were unable to include all of the variables in a single MANOVA model due to the 140missing values generated as plants died. For survival, we analyzed the number of days to death 141for all plants. For total number of seeds, we included starting height as a significant covariate. 7 142We removed those plants that had died within 8 weeks of transplant, as seed production was 143essentially non-existent up to that time. For final height and stem diameter, we used a MANOVA144with starting height as a significant covariate for the 32 surviving plants. When significance was 145found in the MANOVA using Wilk’s λ, we ran separate univariate Analyses of Variance 146(ANOVAs) for each variable. For all statistical tests, model assumptions of normality and 147heteroskedasticity were verified prior to analysis and transformed where appropriate.148149150151 Results and Discussion152153 We wanted to know if the putative invasive R. ficaria negatively affected the growth and 154reproduction of the native I. capensis, and if it did, whether allelopathy or nutrient competition 155played a causative role. Because R. ficaria has been identified as invasive (Axtell et al. 2010) 156and has been associated with reduced native abundance and diversity (Homann 2005), we 157expected that the presence of R. ficaria would have a negative impact on the performance of I. 158capensis. Our results show that R. ficaria does indeed negatively affect I. capensis, providing 159confirmatory evidence of its assumed impact on native species. Ranunculus ficaria showed a 160tendency to have a negative overall impact on the survival of I. capensis with plants dying ~10 161days earlier in the presence of R. ficaria (F1,55 = 3.75, p = 0.058; Figure 1). In the absence of 162carbon, R. ficaria decreased seed production by ~50% (Figure 2). 163 As expected, addition of nutrients showed a significant effect on growth (in terms of 164height and stem diameter) and seed production. For the total number of seeds produced, there 8 165was a significant effect of nutrient addition (F1,47 = 20.53, p < 0.001). The presence of nutrients 166nearly tripled seed production (Figure 3). In the MANOVA, there was a significant effect of 167nutrient addition on final height and stem diameter (F2, 22 = 14.904, p = 0.000). In the univariate 168ANOVA, addition of nutrients increased both height (F1, 23 = 7.28, p = 0.013) and stem diameter 169(F1, 31 = 30.34, p < 0.001) (Figure 3). If nutrient competition were a key factor in inhibition of I. 170capensis by R. ficaria, we would have expected I. capensis to exhibit a release from competition 171in the presence of added nutrients. There was no significant interaction between nutrient addition172and presence of R. ficaria, suggesting that nutrient competition was most likely not the primary 173mechanism of impact of R. ficaria. We do however acknowledge that our study does not rule 174out other forms of resource competition, such as competition for light or water.175 There was a significant interactive effect between R. ficaria-presence and carbon (F1,47 = 1765.03, p = 0.030). When carbon was absent, the presence of R. ficaria reduced seed production. 177When carbon was present, seed production was similar whether R. ficaria was present or absent 178(Figure 2). Carbon therefore ameliorated the negative effect of R. ficaria on I. capensis. In 179previous research, application of carbon to soils has mitigated the effects of invasive species 180(Cipollini et al. 2008a; Ridenour and Callaway 2001). Ridenour and Callaway (2001) found that 181the competitive ability of Eurasian grass species was greatly reduced by activated carbon and 182suggested that the advantage of this species, at least in part, was due to allelopathy. Similarly, 183one possible conclusion from our study is that the addition of carbon may have attenuated the 184allelopathic effect of R. ficaria. However, when using activated carbon as an experimental tool to185test allelopathy, caution must be used in interpreting results. The addition of activated carbon 186itself can change soil conditions in potting soil (Lau et al. 2008; Weisshuhn and Prati 2009), 187though these studies used twice as much activated carbon compared to the amount used in our 9 188study. Activated carbon itself can have a direct fertilizing effect (Lau et al. 2008). In our study, 189the mitigating effect of carbon was significant even in nutrient-addition treatments, suggesting 190that direct addition of nutrients by the activated carbon was most likely not the mechanism 191through which carbon exerted its effects. Ranunculus ficaria is purported to have medicinal uses 192in herbal medicine as a treatment for hemorrhoids and as an astringent (Chevallier 1996) and 193contains a number of secondary chemicals (Texier et al. 1984; Tomcysk et al. 2002). The 194presence of secondary compounds may be a good predictor of invasive species impacts, 195including allelopathy (Ehrenfeld 2006). Further, because R. ficaria exhibits direct allelopathy on 196some species in the laboratory and greenhouse (K. A. Cipollini, personal communication), 197allelopathy is a likely mechanism in the field, though clearly further study is needed (see Blair et 198al. 2009). Whatever the exact mechanism of its effect, activated carbon nevertheless was clearly 199able to negate the negative effect of R. ficaria, suggesting that, at the very least, it may serve as 200an effective restoration tool to modify soil conditions in the field to the benefit of native species 201(Kulmataski and Beard 2006; Kulmatiski 2010). 202 Interestingly, we found that R. ficaria had lasting effects beyond its brief growing season.203We expected that effects on I. capensis would not be particularly strong, as it is thought that the 204negative effects of this species are exerted primarily on spring ephemeral species (Swearingen 2052005). Further studies using spring ephemeral species are obviously needed to clarify the 206comparative effect on this set of species presumed most sensitive. Even though R. ficaria had 207completely senesced by week 6 of the experiment, it still significantly negatively impacted I. 208capensis, which lived without the presence of R. ficaria for about two-thirds of its life span. 209Other invasive species can have residual effects on native species, even after the removal of the 210invasive species (Conser and Conner 2009). The effect of R. ficaria well past its growing season 10 211may be due to lingering effects, such as those due to allelochemicals or to other modification of 212soil conditions. An alternative explanation may be that the seedling stage is the most vulnerable 213stage of I. capensis, similar to the findings in Barto et al. (2010). 214 Despite its widespread identification as an invasive species, this is the first study to show 215the negative impact of R. ficaria on I. capensis and to point towards a possible mechanism of 216success – allelopathy or other modification of soil conditions. It is surprising that this is the first 217published study to investigate the invasive potential of R. ficaria, given that natural resource 218agencies have recognized it as a species important to control in natural areas since at least the 219year 2000 (Hammerschlag et al. 2002). Ranunculus ficaria has already been banned in two states220(Axtell et al. 2010) since the year 2006. Admittedly, there is a balance between taking immediate221action against an invasive species and waiting for time-consuming scientific studies (Blossey 2221999). Indeed, we support the use of the “precautionary principle” (e.g., Blossey 2001) in 223assessing invasive species. Since R. ficaria can form dense monocultures, the assumption that it 224is an invasive species is most likely a valid one. However, in the ten or more years it has been 225identified as a concern, there is not a single published paper documenting its impact. It is entirely226possible that the impact of R. ficaria has been overblown in the eyes of the public (Lavoie 2010),227causing larger-than-needed economic losses to the horticultural industry and redirection of 228resources away from more important invaders. This research provides an example of the need for229more basic research into invasive species impacts and mechanisms of impacts on native species 230for use in effective invasive species targeting, control and management. 23123223311 234 Sources of Materials2352361 Aquarium Pharmaceuticals Black Magic Activated Carbon, Chalfont, PA, USA2372 Scotts-Sierra Horticultural Product Co., Marysville, OH, USA238239240241 Acknowledgments242243 We would like to thank Kyle Titus and Sara Moore for assisting in field research. We 244also thank Doug Burks, Don Troike, and Doug Woodmansee who provided guidance throughout 245this project. We thank Don Cipollini for his insight and support. 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Mean (± SE) number of seeds, height and stem diameter of Impatiens capensis grown 388with and without nutrients, across Ranunculus ficaria and carbon treatments. 389390 39139239339439539639739839940040140219 120110 p = 0.058 s 100 y a d90 n i n 80 a p s 70 e f i 60 L5040 - R. ficaria + R. ficaria 40320 40440520 - R. ficaria p = 0.030 18 + R. ficaria s 16 d e e 14 s f 12 o r e 10 b m 8 uN 6 4 2- Carbon + Carbon 40640721 25 p < 0.001 20 s d e e s 15 f o r e b 10 m u N 50 50 p = 0.013 40 m c30 n i t h g i 20 e H100 0.8 p < 0.001 m c 0.6 n i r e t e 0.4 m a i d m e t 0.2 S0.0 - Nutrients + Nutrients 40822 409 Interpretive Summary410411 Lesser celandine (Ranunculus ficaria) has been considered an invasive species and has even 412been banned from sale in some states. However, there is no scientific research confirming its 413negative impacts. In this study, we aimed to determine the impacts of lesser celandine on 414reproduction, growth and survival of transplanted native jewelweed (Impatiens capensis). We 415also wanted to determine if competition for nutrients or allelopathy (manipulated by the addition 416of activated carbon) played a role in its presumed invasive success. In the field, we manipulated 417the presence or absence of lesser celandine, nutrient addition and activated carbon in a fully-418factorial experiment. The addition of nutrients increased seed production, height and stem 419diameter of jewelweed. However, there was no interactive effect of the presence of lesser 420celandine and nutrient addition, suggesting that superior nutrient competition is not the 421mechanism through which lesser celandine exerts its effects. The presence of lesser celandine 422tended to reduce survival of jewelweed. In the absence of carbon, lesser celandine reduced seed 423production of jewelweed, while the presence of carbon mitigated this negative effect. While 424there are some issues with using activated carbon to study allelopathy, these results, combined 425with our unpublished laboratory data on allelopathic effects of lesser celandine, point towards 426allelopathy as one plausible mechanism of lesser celandine’s negative impact. Further, it has 427been hypothesized that lesser celandine has impacts primarily on spring ephemerals. Lesser 428celandine exerted its impacts well beyond its ephemeral growing period, as lesser celandine grew429with jewelweed for only one-third of jewelweed’s life cycle. This study broadens our 430understanding of the invasive potential of lesser celandine and points towards the need to 431confirm impacts and explore success mechanisms of presumed invasive species.23

Negative Impacts and Allelopathic Potential of the Ephemeral Invasive Ranunculus Ficaria

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